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Medical Hypotheses (2005) 65, 922–931 http://intl.elsevierhealth.com/journals/mehy Neural correlates of consciousness: A definition of the dorsal and ventral streams and their relation to phenomenology Costa Vakalopoulos * 171 McKean Street North Fitzroy, 3068 Melbourne, Australia Received 19 April 2005; accepted 16 May 2005 Summary The paper presents a hypothesis for a neural correlate of consciousness. A proposal is made that both the dorsal and ventral streams must be concurrently active to generate conscious awareness and that V1 (striate cortex) provides a serial link between them. An argument is presented against a true extrastriate communication between the dorsal and ventral streams. Secondly, a detailed theory is developed for the structure of the visual hierarchy. Premotor theory states that each organism–object interaction can be described by the two quantitative measures of torque and change in joint position served by the basal ganglia and cerebellum, respectively. This leads to a component theory of motor efference copy providing a fundamental tool for categorizing dorsal and ventral stream networks. The rationale for this is that the dorsal stream specifies spatial coordinates of the external world, which can be coded by the reafference of changes in joint position. The ventral stream is concerned with object recognition and is coded for by forces exerted on the world during a developmental exploratory phase of the organism. The proposed pathways for a component motor efference copy from both the cerebellum and basal ganglia converge on the thalamus and modulate thalamocortical projections via the thalamic reticular nucleus. The origin of the corticopontine projections, which are a massive pathway for cortical information to reach the cerebellum, coincides with the area typically considered as part of the dorsal stream, whereas the entire cortex projects to the striatum. This adds empirical support for a new conceptualization of the visual streams. The model also presents a solution to the binding problem of a neural correlate of consciousness, that is, how a distributed neural network synchronizes its activity during a cognitive event. It represents a reinterpretation of the current status of the visual hierarchy. c 2005 Elsevier Ltd. All rights reserved. Introduction A theory of premotor relations discusses the emergence of cognitive processes and conscious awareness from the motor history of a developing * Tel.: +61408810220. E-mail address: [email protected]. organism [1]. It is mediated by a mechanism of motor efference copy, which directly modulates the neural properties of neocortical regions receiving perceptual input from the respective sensory organs. It ascribes meaning to this input determining the quality of the experience. A notable feature of neocortical networks is a division of processing between dorsal and ventral streams and is best described in the pri- 0306-9877/$ - see front matter c 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.mehy.2005.05.016 Neural correlates of consciousness mate visual hierarchy. The dorsal stream is often described as the ‘where’ pathway serving spatial information that allows us to navigate the environment or pick up an object. The ventral stream, on the other hand, serves object recognition, the so-called ‘what’ pathway. This concept of brain architecture is supported by local lesion studies. Remarkable progress has been made over the last several decades delineating visual areas according to physiological properties and anatomical connections. The research effort has culminated in detailed maps of the interrelation of the various subregions within a dorsal/ventral stream framework.The benchmark paper is by Felleman and Van Essen [2]. However, there are a number of contentious debates surrounding the accuracy of these maps and their exact significance for cognitive function. The first part of this paper will deal with a hypothesis of a neural correlate of consciousness. The modern concept is of a widely distributed network, but the relative and critical importance of the striate cortex and frontal lobes is in great dispute.The problem has become so intractable that Milner and Goodale even propose a third pathway based on lessons learned from the neglect literature. The first hypothesis of the present paper states that concurrent activation of both dorsal and ventral streams are required for conscious awareness. From a theoretical point of view,this is a prediction of premotor theory since both streams present the totality of categorization of motor efference copy of the exploring organism. From the empirical stance evidence supporting this contention is gained from direct electrical stimulation of the temporal cortex (ventral stream) and supplemented by lesion studies of the parietal cortex (dorsal stream). The second part of the paper deals with the fine structure of the visual hierarchy by proposing heuristic definitions of the dorsal and ventral streams. The status of the lateral connections between regions and the flow of information between the two pathways present prescient anomalies to the currently favoured model. Premotor theory states that each organism–object interaction can be described by the two quantitative measures of torque and change in joint position. This leads to a component theory of motor efference copy providing a fundamental tool for categorizing dorsal and ventral stream networks. The second main hypothesis then, states that a rigorous definition of the visual hierarchy is based on the distribution of cortical projections to the cerebellum and basal ganglia, the former uniquely determining dorsal stream properties and the latter a characteristic of both streams.The aforementioned structures code for 923 the parameters of change in joint position and torque conditions of an interactive history, respectively [1]. The model renders the concept of lateral connections obsolete. The third major hypothesis proposes a mechanism of binding of distributed neural networks. The thalamic reticular nucleus TRN envelops the entire thalamus and can mediate the binding by a motor reentrant pathway through its known modulation of thalamocortical networks. It directly addresses the important philosophical issue of embodiment of phenomenal experience in spite of a non-focal neural correlate of consciousness. Neuroanatomical correlates of consciousness Ungerleider and Mishkin [3] showed that object recognition and spatial tasks were served by cortical pathways and that these projected differentially to the inferior temporal (IT) and posterior parietal cortex, respectively. A practical argument will be made that the awareness of a phenomenal episode requires the simultaneous activation of the dorsal and ventral streams described here as parallel premotor levels. The reciprocal nature of cortical networks is consistent with the paradigm view of a non-focal localization of awareness. However,the striate cortex appears to play a unique role in visual awareness and premotor theory proposes that it serves as a serial link between the streams. Certainly, attention appears to modify activity within both extrastriate and striate cortex as shown by binocular rivalry experiments [4,5]. The significance of these studies is that they suggest that early visual cortex is not simply a passive receptacle. The hypothesis is that true reciprocal pathways between the dorsal and ventral streams exist only in the region of the striate cortex. This opinion is obviously contrary to current beliefs and will require justification. It is in considering the pathways for top-down generation of imagery that the serial nature of the structure of the striate cortex becomes apparent. There is substantial evidence for an overlap of networks that serve both bottom-up and top-down processes, i.e., internal images use homologous neural networks to those directly representing the same external event. It is proposed that the production of a top-down image requires the serial activation of the dorsal stream via ventral backprojections to the striate cortex. At progressively higher levels individual neurons exhibit greater subspecificity. The underlying structure of the visual 924 Vakalopoulos posterior parietal cortex (dorsal stream) striate cortex V1 inferior prefrontal cortex inferior temporal cortex (ventral stream) Thalamus (eg MDmc) lateral hypothalamus Figure 1 Top-down imagery. hierarchy is an anterior convergence of posterior intraareal elements [6,7]. In the ventral stream,this would facilitate the endogenous stimulation of a focal group of neurons augmenting a response within the inferotemporal cortex and recruiting by backflow primary cortical modules. While probing the exposed cortex of patients during neurosurgical procedures for epilepsy in the 1940s, Wilder Penfield showed that direct stimulation of the temporal lobes evoked explicit memories. Premotor theory predicts that an image is evoked by linking of the ventral to the dorsal streams at the level of the striate cortex (Fig. 1). That the dorsal stream is a critical element of conscious perception is suggested by the syndrome of unilateral neglect, which is associated with lesions of the inferior parietal lobule and is clinically demonstrated by a lack of awareness of contralateral space. Critically, the deficit can manifest itself in imagination,such as when patients are asked to recall a familiar scene [8]. The evidence from Penfield’s studies and patients with neglect thus, suggest top down pathways from temporal cortex (ventral stream) recruits posterior or inferior parietal (dorsal stream) networks in the evocation of imagery. Lesions in striate cortex that result in blindness also impede the resolution of cognitive imagery, suggesting that V1 is the critical binder of parallel streams of premotor level functions. Whether conscious vision is possible without V1 is still hotly debated. Premotor theory does not imply that visual awareness is localized to V1, but only that it is a critical link within a distributed neural correlate. Consistent with this view neuroimaging studies demonstrated activation of human primary visual cortex [9] and the lateral geniculate nucleus [10] during visual recall.In fact, in a visual imagery task of famous faces, cortical activation involved a distributed network including the intraparietal sulcus and temporal cortex in addition to the striate cortex [11]. The theory still allows that under pathological conditions dorsal and ventral stream binding may generate a conscious percept independent of V1 activation. For example, LSD, a 5HT2 receptor agonist, induces visual hallucinations with prominent parietal and temporal lobe activation and relative striate cortex inactivation [12]. A similar argument can be made for dreaming where PET studies have shown significant activation of the inferior parietal lobe and inferior temporal cortices, in addition to limbic and paralimbic areas, but relative inactivation of V1 (see review in Hobson et al. [13]). Component theory of motor efference copy Torque and change in joint position are the two parameters that specify all motor activity including Neural correlates of consciousness velocity and acceleration. Motor reentry can be analyzed as a component theory of motor efference copy serving distinct cognitive parameters in the organization of neocortical networks. It is not intuitively obvious parameters of a motor action can specify the properties of posterior cortical regions one tends to associate with object or face recognition, for example. It is precisely this conceptual undertaking premotor theory claims. A detailed exposition of the theory of premotor relations is to be found elsewhere [1]. Conditions of torque in a neural network may conceivably be specified by the basal ganglia via TRN modulation of thalamocortical projections. Whether the role of the basal ganglia can be entirely defined in this manner remains to be demonstrated. However, several extrapyramidal features of patients with Parkinson’s disease support this claim. Signs of bradykinesia are generally considered a deficiency of dopamine regulation within the basal ganglia. A shuffling gait is a characteristic of these patients. A step involves a power burst by an appropriate muscle group. Any movement has accelerating and decelerating phases,which are directly proportional to force exerted. Godaux et al. [14] revealed a diminution in the rate of rise of muscle activity during rapid arm reaching movements to a visual target, but normal sequential activation of muscles, co-contraction of antagonist muscles, movement trajectory and accuracy. There is evidence that the latter parameters, which may be normal in Parkinson’s disease, are served by the cerebellum [15,16]. However, it may not be possible to entirely dissociate kinematic effects from kinetic deficits. Overall,the evidence suggests a failure in force generation associated with basal ganglia pathology. Given its role in force generation, the basal ganglia can thus, specify the torque component of motor efference copy as an organizing principle of neocortical categorization. Majsak et al. [17] showed an impairment in the acceleration phase of reaching for a stationary ball. In a study by Berardelli et al. [18] patients were able to modulate EMG activity during wrist flexion in the same way as normals, but could not use these bursts to make rapid movements. The authors state that: ‘‘The patients appear to underestimate what muscle activity is required for a particular movement. There is a breakdown of the link between perceptual appreciation of what is needed and the delivery of appropriate instructions to the motor cortex ’’. These findings are predicted by a cognitive theory of the basal ganglia. Premotor theory states that the judgment of the force required is an inherent prop- 925 erty of the phenomenology of perception of the object. In a study by Mollion et al. [19] PD patients off medication were differentially impaired in a non-spatial compared to a spatial version of a working memory task based on reaction times. The authors concluded that the deficit could not be attributed to a simple motor impairment and implicating a cognitive role for the basal ganglia. What premotor theory attempts is a conceptual bridge between force generation and cognitive function so that dysfunction of the former underpins impairment of the latter in some fundamental sense, that is it is not just an incidental association [1]. Proprioceptive feedback is the second critical element of premotor category function. Joint position will be served by the cerebellum.The organization of cerebellar global networks parallels that of the basal ganglia [20]. The afferent limb is a massive corticopontine and mossy fibre system. The efferent reentrant limb is a projection of the deep cerebellar nuclei to the motor thalamus.This loop covaries with peripheral cerebellar input. However, the corticopontine network has a restricted origin, with a distinct spatial character, in contrast to the widespread input to the striatum [21]. Its distribution of origin appears to parallel the areas commonly attributed to the dorsal stream, especially parietal cortex. The cerebellar loop fulfils the criteria of a spatiotemporal relation to the organism and which can only be specified by changes in joint position during an interactive history. Conversely, the categorization of a percept in the inferotemporal cortex is not spatial, but feature-dependent. Recognition is generally, orientation insensitive, eschewing a proprioceptive role in the organization of ventral stream circuits that serve it and which project predominantly to subcortical hedonic centres rather than dorsal prefrontal and motor areas to which the dorsal stream projects. Receptive field properties of the ventral stream are tolerant of various spatial loci and orientations for an object. This cannot be the case for accurate visuomotor control that is the presumed function of the dorsal stream. A clearly stated hypothesis is that corticopontine projections as part of the cerebellar loop define a priori the dorsal stream of any modality. This appears quite satisfying intellectually because dorsal stream function is generally associated with spatial localization and the cerebellum can directly specify the neocortical neural properties that encode such knowledge. That is,the target of a visually guided movement must already have an inherent algorithm as part of the phenomenological 926 Vakalopoulos awareness of the object for the correct movement to be executed. Ventral/dorsal stream boundaries Several visual areas assigned to the dorsal stream by most current descriptions of the visual hierarchy appear to have connections with the ventral stream as illustrated by the middle temporal (MT) and superior temporal polysensory (STP) [22,23]. The projections to the ventral stream from these classic dorsal stream areas (especially MT) may come from a distinct ‘ventral’ subpopulation involved in the recognition of moving objects, STP possessing neurons whose activity is specific for movements such as walking [24]. This serves the ventral stream function of recognition that a subject is walking,for example. It may be misleading to consider this a true exchange between the parallel streams given the current disagreement on what areas constitute the dorsal stream [25]. Premotor theory gives a functional definition of the dorsal and ventral streams based on properties of subpopulations of neurons, but which do not necessarily correspond to an areal distribution. An area such as MT, which is classically regarded as part of the dorsal stream will, according to a component theory of motor efference copy, possess two subpopulations of neurons, only one of which has properties that define the dorsal stream. These properties are the presumed product of the cerebellar loop. The other group has receptive field properties specified by the basal ganglia and is a constituent of both ventral and dorsal streams. It is only the latter neuronal type that is proposed to have reciprocal connections between areas that are typically regarded as being segregated in parallel streams. In other words, it may be more accurate to consider that the parallel nature of the respective streams is maintained within a particular domain or visual area. Fig. 2 and the discussion in the next section will make this point clearer. Current staining techniques may not reveal the heterogeneity in the neuronal properties of a particular visual area with only a subpopulation being the potential source of the corticopontine efferents. Studying the figures of Schmanmann and Pandya [21] one is struck by how the shaded area (origin of the corticopontine projections) delineates a sharp boundary in the superior temporal sulcus (STS) separating parietal cortex from the non-shaded inferotemporal cortex (ITC). The apparent homogeneity of the shading belies the possible functional differences of subpopulations of neurons within these Figure 2 Dorsal and ventral streams. A schematic figure of the distribution of neuronal subpopulations (crosses and ovals) in the ventral and dorsal streams of the monkey visual cortex. The dashed line represents the limits of the superior temporal sulcus. The oval figures are a proposed category product of the cerebellar loop. They code for spatial coordinates and are modulated by gaze direction. Their distribution corresponds to the shaded corticopontine projection areas of Fig. 4 in Schmahmann and Pandya [21]. The crosses comprise the proposed neuron population categorized by the basal ganglia and represents the torque conditions of their receptive field properties. These neurons are found in PPC, STP and IT. It is only this subgroup that projects to both dorsal and ventral streams. The dorsal and ventral streams according to this model are defined by the physiological properties of neurons and not any strict anatomical demarcation. The receptive field properties of both subpopulations ultimately combine in a motor transformation that represents the parameters of pyramidal motoneurons. In the proposed convergence of dorsal stream receptive fields the torque condition may be specified by any of the red marked population [An analogous pattern of distribution can be extrapolated for the prefrontal cortex dorsal and ventral to the principal sulcus]. shaded areas, as already stated. None the less, the general correspondence of the shaded area to the dorsal stream pathways is so striking, it gives unequivocal support for a component premotor definition of the visual hierarchy. The arrangement of projections from the basilar pontine nuclei to the cerebellum implies that a focal cerebral cortical area is distributed to numerous discrete sites in the cerebellum and conversely, that many cerebral areas communicate with a single folium [21]. The basilar pons distributes its mossy fibre terminals predominantly to the lateral cerebellar hemispheres [26]. The interaction of mossy fibre input to the cerebellum with the ‘patchy’ mosaic pattern of climbing fibre input evoked by peripheral somatosensory input sub- Neural correlates of consciousness serves the putative cognitive function of dorsal stream-type networks. The inferior olive is the origin of climbing fibres to the cerebellum and each purkinje cell has input from both systems (mossy and climbing fibres). Thus, the peripheral sensory input to the olive is in a unique position to modulate the activity of the cerebropontine projection system. This will not be a simple facilitation of mossy fibre activity, but an imposed specification of cortical network properties by association of perceptual information with a history of component motor efference copy. The contextual interactions between these two systems were originally proposed in an instruction-selection theory of cerebellar learning [27], but the cognitive role of the cerebellum has only more recently been the focus of speculation. One might expect the neocerebellum (much expanded in primates) to play a dominant cognitive role in spatial awareness! A detailed structure of the visual hierarchy For a particular premotor act and its corresponding premotor levels, the cortical pathways through various visual areas are bound by a specific motor history and its motor efference copy through a common node of reentry, the thalamus. The theory proposes that the ‘perpendicular’ thalamocortical circuits are categorizing and the parallel cortical domains, the substrate categorized. Pallidal projections to thalamocortical circuits are the proposed pathways for the categorization of the visual hierarchy. The complex cells of the striate cortex are already exhibiting some of the receptive field properties of neurons at more anterior levels of the visual hierarchy. Binocular V2 neurons respond to illusory contours. MT (V5) detects motion. V4 is the colour area. Lesions in these two areas cause deficits in perceiving motion and colour, respectively. Within each domain of a sensory hierarchy neurons display category specific properties which are a unique,although not an exclusive, innovation for that domain. What is the neuroanatomical basis for the introduction of category specific function? The associative visual cortices project to the striatum with a variable degree of segregation. The topography of specific regions of the thalamic nuclei, such as the pulvinar has largely segregated corticothalamic projections [28]. Thus, the parallel anatomical arrangement allows the process of motor reentry (motor efference copy) to functionally differentiate the corticostriatal, 927 thalamocortical loops that project to and from the various visual areas V2,V3,V4, MT, etc. This is proposed to be the origin of the characteristic properties of individual areas within the visual hierarchy as one progresses from posterior to anterior cortex. The properties of neurons in the visual hierarchy become progressively more complex, even abstract, yet are the outcome of a reductive process of a thalamocortical axis of reentry. In addition, contrasting sequences of motor activity, for example, may categorize the neural assemblies that are conscious of an object,or of facial features in both specific spatiotemporal coordinates (posterior parietal cortex) and non-spatial recognition circuits (inferotemporal cortex) via corticopontine and corticostriatal loops, respectively. A component motor theory of reentry provides torque as a sole condition for ventral stream networks as is the case for the posterior inferotemporal cortex. In other words, the role of the ventral stream in object and facial recognition is developmentally linked to the basal ganglia only. The cerebellar loop, on the other hand, provides a spatiotemporal history. In summary, the mechanism of motor reentrant function may characterize both the properties of individually defined areas as one ascends the visual hierarchy and the division of visual processing into dorsal and ventral streams. Neuroanatomical evidence supports the role of the thalamocortical projection in the categorization cortical neuronal properties. Ascending intercortical connections is associated with the convergence of receptive field properties. Neurons in more anterior locations of the visual cortex have larger even bilateral fields suggesting a cumulative response. Convergence of neuronal types is postulated and has been demonstrated anatomically by the lateral connections of supragranular and, to a lesser extent, infragranular clusters of interdigitating columns or modules of a visual area [29]. Pulvinocortical connections with extrastriate visual areas project predominantly to layer 3 with axon collaterals to other depths which are often not in register with the typical columnar organization [30]. Clustered terminal arbors distributed within a visual area may form a mechanism for the conjoint effects of motor efference copy on disparate intraareal elements. This demonstrates how motor reentry can bind the properties of distinct intraareal neuron clusters. The final section will deal with how non-contiguous visual areas can form a distributed neural network, functionally coupled into a single cognitive domain or event. This has been coined the binding problem, i.e., how a distributed networks that serves conscious awareness can be bound into a functional unit. But first, a 928 Vakalopoulos demonstration of how premotor theory can resolve several key problems in the current scheme of the visual hierarchy is discussed. The currently accepted map of visual areas will be described as the old model to distinguish it from a new paradigm presented here. Anomalies of the visual hierarchy In a detailed analysis of the relationship between visual areas based on the origins and terminations of laminar cortical projections, Felleman and Van Essen [2] placed areas at the same level if the projection was columnar and ascending if predominantly to layer 4. Furthermore, a commonly held belief is that the dorsal and ventral streams communicate in prestriate cortex. This certainly fits the dominant view of a compartmentalization of parvocellular and magnocellular pathways as the predominant inputs to ventral and dorsalstreams, respectively. However, functionally there is evidence for mixing of these signals [31]. The latter findings are consistent with the alternative interpretation offered here that a typically parvocellular feature such as colour contrast must be processed in both a spatial (posterior parietal) and an object (inferotemporal) sense. The treatment of visual areas in this manner may help resolve the potential anomalies of the visual hierarchy. This is exemplified by the reciprocal relationship of cortical areas such as the dorsal medial superior temporal (MSTd) and 7a and the ambiguity inherent in the projections from MT to V4 [2,32] MSTd projects to area 7a as a columnar pattern (C). The projection from posterior parietal 7a to MSTd is a multilayered pattern (M) typical of a backprojection, (Fig. 3). Under the old model a columnar pattern is a lateral projection (same level in the hierarchy) and the expectation would be a columnar pattern for the reciprocal projection. But, this is multilayered (projections to supragranular and infragranular layers), which is typical of backprojections, directly contradicting the lateral connection model. The basic premise of the new model is that columnar patterns are part of the anterior projection crossing various domains in a hierarchical model, without the need to invoke lateral connectivity. Visual areas need not be assigned exclusively to a dorsal and ventral pathway, but may have elements inclusive of both. Similar to the above interpretation, the V4 to MT columnar projection is destined for a dorsal category stream and thus an apparent change in stream from a ventral to dorsal premotor level. However,MT has two patterns of reciprocal projections with V4. One is columnar as the same level hypothesis predicts (old model), but the other is multilayered, typical of a backprojection, an untenable finding for the old model. The most parsimonious explanation is to regard these connections as part of two parallel networks within the ventral and dorsal streams, respectively (Fig. 4). This requires a change in point of view that neither MT nor V4 are entirely defined by a single stream. Thus, there is no requirement for a communication between the parallel streams. According to the old model, the ascending pathway is defined by a prominent layer 4 input. The new model maintains this, but considers uniform columnar interdigitation a variation on the same theme, without invoking the problematic view of lateral connections. By admission of the authors themselves [2], most suggested lateral connections are problematic at Parietal Temporal Anterior C V4 MT M M 7a MSTd C Striate Cortex Posterior Figure 3 Lateral connection between MSTd and 7a. Figure 4 Lateral connections between V4 and MT. Neural correlates of consciousness some level of description, but the acceptance of their existence as can be discerned from the scientific literature contradicts this irresolute ambiguity. In the case of V4 and MT, laterality is suggestive of a complete and reciprocal transfer of information between both the dorsal and ventral streams. An alternative paradigm proposes that only neuronal populations that are the category products of the basal ganglia and hence, the torque component of motor efference copy, will be represented in either stream. A particular area, such as MT or MST will have a population of neurons with properties specified only by the basal ganglia and these will be distributed in parallel. Conversely, neuronal populations that are the category products of the cerebellar loop and hence, the change in joint position component of motor efference copy, are exclusive of the dorsal stream by definition and do not project to the ventral stream (Fig. 2). The inference that can be drawn from this model is that although, there is an obvious exchange of information between extrastriate areas such as V4 and MT,this does not necessarily assume a communication between streams. An individual domain may contribute to the neural processing of both ventral and dorsal streams in a parallel fashion. The existence of only a subpopulation within the parieto-occipital cortex that is responsive to changes in the direction of gaze is compatible with this view. In extrastriate area V3A, for example, the responsiveness to visual stimulation of only about half of the studied units was modulated by the angle of the experimental animal’s gaze [33]. These neurons are presumably involved in the coding of spatial coordinates. Furthermore, gaze dependent neurons appear to be segregated from non-gaze dependent cells in the same cortical area. Similar proportions of gaze and non-gaze dependent neurons are found in area V6 [34], where they are more uniformly distributed, and area 7a [35]. The hypothesis is that the differential modulation of receptive field properties may be attributed to their respective projections to either the striatum or basilar pons representing the pathways for the categorization by the two respective components of motor efference copy, torque or force and joint position. 929 many parts of the brain may be physiologically coupled in a neurobiological correlate of consciousness. Essentially, the hypothesis is based on a principle of self-organizing behaviour of thalamocortical assemblies. Premotor theory takes a further step in proposing that the organization of cortical networks is a type of embodiment that does not require the statistically improbable state of strictly synchronized activity to provide a sense of unity. Each neocortical category domain of a sensory (visual) hierarchy projects reciprocally to a subsequent category domain or visual area. The primary architecture is epigenetically determined. Contiguity of cortical areas ultimately bears on shared physiological roles, but prolific reciprocal connections are shared by areas that are quite distant from each other, such as the prefrontal region dorsal to the principal sulcus and the posterior parietal cortex. Areas that are reciprocally bound may be considered as nodal points in a proposed triad of motor reentry. The model of triangulation purports the hierarchical binding of specific networks within the visual cortex by non-overlapping motor relations. The third nodal point is subcortical within the structure of the thalamus (Fig. 5). Cortical nodes have widely distributed reciprocal networks creating a 3-dimensional lattice. There is apposition of the largely segregated cortical prefrontal and posterior parietal domains in the medial pulvinar and their extension across the mediodorsal thalamic border [37]. The corticothalamic projection zones of some areas with reciprocal inputs such as MT and V4 do not overlap at all [7]. Critically, the corticothalamic projections have a topographic order, with scant evidence of intrinsic interthalamic Parietal Prefrontal TRN Model of triangulation Recent theoretical interest in the synchronization of neuronal firing patterns has been advocated as a solution to the binding problem of consciousness [36]. That is, how neural networks distributed over Motor Feedback Pulvinar Figure 5 Binding model of triangulation. 930 connections. This poses the main problem as I see it for a binding mechanism of different neuronal populations, which is solved by a model of reentry that proposes the mediation of pallidal afferents within and across thalamic borders. Small biocytin injections in GPe resulted in profuse anterograde labeling of fibres within the entire rostrocaudal extent of the TRN [38]. The labeled fibres were long and gave off numerous short collaterals that terminated in clusters of large varicosities. Thus, this projection is ideally placed for the ‘synchronous’ modulation of segregated thalamocortical groups. Conclusion The application of premotor theory to brain structure and function could prove a useful tool for establishing a rigorous definition of the visual hierarchy. The theory provides a fundamental mechanism of binding and how a distributed network can still have a sense of embodiment of the phenomenal experience without invoking a regressive homonculus. The dorsal and ventral streams can be modeled on the reentrant input from cerebellar and pallidal projections to thalamocortical circuits, respectively. If correct, it will lead to a radical change in thinking about the functional underpinnings of the neocortex and the significance of the basal ganglia and cerebellum in the cognitive domain. It will require a reappraisal of the currently published maps of the visual hierarchy. It will also lead to a better understanding of the cognitive and psychiatric dysfunction associated with disorders of these structures, such as Huntington’s and Parkinson’s disease. Further empirical support for the theory can be gained by animal studies using reversible inactivations of these structures and observing consequences of cognitive function. Non-invasive studies on humans using new TMS technology could achieve similar results. Further descriptions of the intrinsic properties of visual cortical neurons by intracellular recording techniques along the lines of the motor parameters torque and proprioception suggests a novel experimental paradigm. References [1] Vakalopoulos C. A scientific paradigm for consciousness: a theory of premotor relations. Med Hypoth [in press]. [2] Felleman DJ, Van Essen DC. Distributed hierarchical processing in the primate cerebral cortex. Cerebral Cortex 1991;1:1–47. Vakalopoulos [3] Ungerleider LG, Mishkin M. Two cortical visual systems. 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